Over-Expression of UV-Damage DNA Repair Genes and Ribonucleic Acid Persistence Contribute to the Resilience of Dried Biofilms of the Desert Cyanobacetrium Chroococcidiopsis Exposed to Mars-Like UV Flux and Long-Term Desiccation

Abstract

The survival limits of the desert cyanobacterium Chroococcidiopsis were challenged by rewetting dried biofilms and dried biofilms exposed to 1.5 × 103 kJ/m2 of a Mars-like UV, after 7 years of air-dried storage. PCR-stop assays revealed the presence of DNA lesions in dried biofilms and an increased accumulation in dried-UV-irradiated biofilms. Different types and/or amounts of DNA lesions were highlighted by a different expression of uvrA, uvrB, uvrC, phrA, and uvsE genes in dried-rewetted biofilms and dried-UV-irradiated-rewetted biofilms, after rehydration for 30 and 60 min. The up-regulation in dried-rewetted biofilms of uvsE gene encoding an UV damage endonuclease, suggested that UV-damage DNA repair contributed to the repair of desiccation-induced damage. While the phrA gene encoding a photolyase was up-regulated only in dried-UV-irradiated-rewetted biofilms. Nucleotide excision repair genes were over-expressed in dried-rewetted biofilms and dried-UV-irradiated-rewetted biofilms, with uvrC gene showing the highest increase in dried-UV-irradiated-rewetted biofilms. Dried biofilms preserved intact mRNAs (at least of the investigated genes) and 16S ribosomal RNA that the persistence of the ribosome machinery and mRNAs might have played a key role in the early phase recovery. Results have implications for the search of extra-terrestrial life by contributing to the definition of habitability of astrobiologically relevant targets such as Mars or planets orbiting around other stars.

Genome-Wide Identification and Bioinformatics Characterization of Superoxide Dismutases in the Desiccation-Tolerant Cyanobacterium Chroococcidiopsis sp. CCMEE 029

“…This was in agreement with the similarities reported for DNA repair proteins of Chroococcidiopsis sp. CCMEE 029 (Mosca et al, 2019(Mosca et al, , 2021 and trehalose and sucrose biosynthetic enzymes (Fagliarone et al, 2020). Indeed, the unicellular Chroococcidiopsis genus and filamentous, heterocystdifferentiating cyanobacteria were reported to be each other's closest living relatives (Fewer et al, 2002).…”

Photoprotection in lichens: adaptations of photobionts to high light

“…Expression analysis of the genes responsible for repair of UV-induced DNA damage, including a photolyase encoding gene (phrA), showed that repair of UV-induced DNA damage contributes to the repair of desiccation-induced damage (Mosca et al . 2019).…”

Exploiting a perchlorate-tolerant desert cyanobacterium to support bacterial growth for in situ resource utilization on Mars

“…Although the strategies to withstand the above mentioned conditions have not been fully deciphered, for Chroococcidiopsis sp. CCMEE 029 the following mechanisms have been identified: (i) avoidance of protein oxidation during air-drying and ionizing radiation (Fagliarone et al ., 2017); (ii) accumulation in response to desiccation of sucrose and trehalose that stabilize dried sub-cellular components, including ribosomal RNA and mRNAs codifying DNA repair proteins (Mosca et al ., 2019; Fagliarone et al ., 2020); and (iii) over-expression of DNA repair genes upon rehydration of dried cells exposed to a Mars-like UV flux (Mosca et al ., 2019).…”